See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/227986529

Are epiphytes important for birds in coffee plantations? An experimental

assessment

Article  in  Journal of Applied Ecology · December 2004

DOI: 10.1111/j.1365-2664.2004.00983.x

CITATIONS READS

125 162

2 authors:

Andrea Cruz-Angón Russell Greenberg

Comisión Nacional para el Conocimiento y Uso de la Biodiversidad Smithsonian Institution
26 PUBLICATIONS   1,005 CITATIONS    122 PUBLICATIONS   6,814 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

National Biodiversity Strategy 2016-2030 View project

Population Ecology View project

All content following this page was uploaded by Andrea Cruz-Angón on 04 June 2018.

The user has requested enhancement of the downloaded file.

Journal of Applied
Are epiphytes important for birds in coffee plantations?
Blackwell Publishing, Ltd.

Ecology 2005
42, 150–159 An experimental assessment
ANDREA CRUZ-ANGÓN* and RUSSELL GREENBERG†
*Instituto de Ecología, AC Departamento de Ecología Funcional, Km 2·5 antigua carretera a Coatepec, no. 315,
91070, Xalapa, Veracruz, Mexico; and †Smithsonian Migratory Bird Center, National Zoological Park, Washington,
DC 20008, USA

Summary
1. Coffee is produced in tropical regions of the world, largely in Latin America. Coffee
cultivation techniques range from traditional systems, where coffee grows under a
diverse canopy of shade trees (shade-coffee plantations), to modern systems, where coffee
grows without any type of shade (sun-coffee plantations). Shade-coffee plantations
provide refuge for forest fauna in otherwise deforested landscapes. The conservation
value of these agro-ecosystems depends upon their structural and floristic diversity.
2. The way coffee producers manage the vegetation, including the epiphytic component,
may profoundly affect the value of plantations for conserving biological diversity. Shade-
coffee certification programmes have emerged to verify that coffee advertised as ‘shade
grown’ is actually grown on highly biodiverse plantations. Although these programmes
universally encourage epiphyte protection from pruning (a common practice), there has
been no experimental evaluation of the importance of epiphytes in supporting faunal
diversity. We report the effect of experimentally removing epiphytes on the bird assem-
blage in a shade-coffee farm near Coatepec, Veracruz, Mexico.
3. We established two matching pairs of epiphyte removal and control plots. We compared
bird diversity and abundance, based on daily censuses during the breeding and non-breeding
season. We used existing information on the way in which birds use epiphytes as foraging
and nesting substrates to explain the presence of different species in plots with epiphytes.
4. Plots without epiphytes tended to be less diverse than plots with epiphytes, but
rarefaction analysis and  showed no significant differences in species richness
between treatments in any of the seasons. Mean bird abundance was significantly higher
in plots with epiphytes during both seasons, and a multidimensional scaling analysis
showed that bird community structure differed between the two treatments.
5. Eighteen forest bird species were significantly more abundant in plots with epiphytes. Three
non-forest species were more common in plots without epiphytes. Resident bird species that
used epiphytes as a nesting substrate were significantly more abundant in plots with epiphytes.
6. When epiphytes are removed, canopy cover, foraging substrates, nest sites and nest
materials are eliminated and microclimatic conditions change. This could increase pre-
dation on adult birds and nests, increase intra- and interspecific competition, and
decrease individual survivorship.
7. Synthesis and applications. This is the first experimental assessment of the import-
ance of epiphytes for birds. Shade-coffee plantations with epiphytes maintain higher
abundance and diversity of the inhabitant bird fauna than plantations without epiphytes.
This study reinforces the value of positive epiphyte management as an important factor in
shade-grown coffee certification, where the goal is to promote biodiversity conservation.
Key-words: biodiversity, birds, community structure, shade coffee management, vascular
epiphytes
Journal of Applied Ecology (2005) 42, 150–159
doi: 10.1111/j.1365-2664.2004.00983.x

© 2005 British Correspondence: Andrea Cruz-Angón, Instituto de Ecología, AC Departamento de Ecología Funcional, Km 2·5 antigua carretera
Ecological Society a Coatepec, no. 315, 91070, Xalapa, Veracruz, Mexico (fax + 52 228 8187809; e-mail angon@ecologia.edu.mx).
151
Introduction
Epiphytes and birds
in coffee Coffee cultivation techniques range from traditional
plantations systems, where coffee grows under a diverse canopy of
shade trees (shade-coffee plantations), to a modern
monoculture, where coffee grows without any type
of shade (sun-coffee plantations). Shaded coffee
plantations provide refuge for forest birds in otherwise
deforested landscapes in the tropics (Aguilar-Ortiz 1982;
Wunderle & Waide 1993; Warkentin, Greenberg &
Salgado-Ortiz 1995; Perfecto et al. 1996; Wunderle &
Latta 1996), especially in Latin America, where coffee
production for export is one of the most important
agricultural activities (Perfecto & Armbrecht 2002).
High levels of structural diversity in the canopy of coffee
plantations are critical for maintaining high bird diver-
sity and abundance (Greenberg et al. 1997; Greenberg,
Bichier & Sterling 1997; Johnson 2000). However, while
emphasis has been placed on the presence or absence
of trees that form an arboreal canopy (Perfecto et al.
1996), epiphytes might also play a critical role in sup-
porting avian biodiversity (Greenberg et al. 1997; Mas
1999; Johnson 2000; Mas & Dietsch 2003).
Planted shade trees such as Inga spp. are colonized
by epiphytes that have dispersed as seeds from nearby
forest or remnant forest trees (Solis 2002). Epiphytes
increase the structural complexity of forests by creating
a variety of supplementary microhabitats and by add-
ing considerable biomass and surface area to the tree
crowns (Remsen 1985; Gentry & Dodson 1987; Sillett
1996; Nadkarni, Merwin & Nieder 2001). Furthermore,
epiphytes can provide birds with nest sites, nest materials
and food in the form of flower nectar, fruit, water, small
vertebrates and invertebrates that inhabit them (Dean,
Milton & Siegfried 1990; Richter 1998; A. Cruz-Angón,
personal observations).
The few studies that have assessed the importance of
epiphyte flora for bird communities in the tropics have
focused on the use of epiphytes by foraging birds dur-
ing just one part of the annual cycle (Remsen 1985;
Nadkarni & Matelson 1989; Sillett 1996; Sillett, James
& Sillett 1997). This approach cannot detect all of the
influences that the presence of epiphytes might have on
bird distribution, particularly indirect effects such as
changes in microclimate. Only experimental removal of
epiphytes can fully assess bird dependence on them.
In this study, we took advantage of a common
management practice (epiphyte removal) in shaded
plantations throughout Latin America (Jones et al. 2000;
A. Cruz-Angón, personal observation) to assess the
importance of epiphytes for birds in these habitats.
There is no clear reason why coffee plantation managers
remove epiphytes from shade trees in their plantations,
although some managers believe that all epiphytes are
parasites that will harm or even kill trees. Many farmers
© 2005 British
Ecological Society,
assume that greater canopy openness and ambient
Journal of Applied light levels will increase coffee yields, but this has
Ecology 42, never been demonstrated as a direct result of epiphyte
150–159 removal. It is clear, however, that epiphyte elimination
results in the structural simplification of coffee plantation
canopies, which could affect the structure and dynamics
of avian communities in these habitats (Greenberg et al.
1997).
In recent years, shade-coffee certification programmes
have emerged to promote ecologically sound manage-
ment among coffee growers and to verify that coffee
marketed as ‘shade grown’ is truly grown on farms with
high structural diversity and adequate resources to
support a diverse associated fauna (Mas & Dietsch
2003). Correlative evidence supports the hypothesis
that epiphytes might be important for canopy faunas
(Greenberg et al. 1997; Mas 1999; Johnson 2000; Stuntz
2001). All the certification programmes consider the
presence of epiphytes to be an important factor con-
tributing to biodiversity, and these programmes require
positive management to promote epiphyte growth
(Mas 1999; Mas & Dietsch 2003). The need to conduct
experimental studies of the value of epiphytes is clear.
Here, we present the first experimental evaluation of
epiphyte influence on bird communities.
Materials and methods
 
Our study site was a 35-year-old, 200-ha shaded coffee
plantation located in Coatepec, Veracruz, Mexico
(19°28′03″N, 96°55′58″W; 1224 m a.s.l.). We selected a
single large coffee plantation rather than several small
coffee farms in order to control for interregional vari-
ation (e.g. weather and altitude). Slope and topography
were uniform throughout the site.
The study farm was a commercial polyculture, the
prevalent management type of coffee plantation in
central Veracruz (Moguel & Toledo 1999). Forest trees
are completely removed, and shade trees, usually nitrogen-
fixing fast-growing legumes such as Inga spp., and
other commercial plant species, such as Citrus spp. and
Musa spp., are planted over coffee (Moguel & Toledo
1999). In central Veracruz, the original forest cover is
tropical montane cloud forest, which since the beginning
of the last century has been replaced by coffee planta-
tions, cattle pastures, sugarcane, cornfields, secondary
vegetation and human settlements (Williams-Linera
2002; Williams-Linera, Manson & Isunza 2002). Although
up to 35 trees species could be found in our study site,
shade was dominated by trees of the genus Inga. Epiphytes
were abundant in the plantation and included bro-
meliads such as Tillandsia schiedeana Steud., Tillandsia
heterophylla E. Morren, and Tillandsia juncea (Ruiz &
Pav.) Poir. as the most common species. The cactus
Rhipsalis baccifera (Mill.) Stearn and the aroid Anthu-
rium scandens (Aubl.) Engl. were also common. Plan-
tation management included herbicide applications
(once a year) and mechanical elimination of weeds
(by machete). Shade trees were pruned every 2 years to
keep shade cover around 60%. Before 1999, epiphytes
were removed from coffee shrubs every 2 years, but
152 Table 1. Descriptive statistics of vegetation surveys done in four experimental plots (treatments) in a coffee plantation in
A. Cruz-Angón & Coatepec, Mexico. Data are mean values ± 1 SE (in parentheses), based on estimates made at five 625-m2 quadrats per plot.
Epiphyte richness surveys were based on 15 Inga jinicuil trees per plot, before workers removed all epiphytes from shade trees in
R. Greenberg
one of two plots at each site (north and south). Treatment: with epiphytes (E+); without epiphytes (E–). Significant differences are
shown with superscript letter (P < 0·0001). NA, information not available

Tree Coffee

Canopy Height Height Density Inga jinicuil Epiphyte

Site Treatment cover (%) Tree ha−1 Species (m) (m) (%) dominance (%) richness

North E– 21·9 (2·6)a 230·4 (62·7) 3·8 (0·2) 7·7 (0·7) 2·1 (0·2) 76·0 (4·0) 56·1 (12·0) 15·9 (0·6)
North E+ 38·7 (5·7)b 262·4 (36·7) 4·2 (0·8) 8·1 (0·8) 1·9 (0·2) 64·0 (4·0) 48·3 (13·9) 15·9 (0·7)
South E– 29·0 (2·3)a,c 172·8 (15·5) 3·2 (0·6) 8·7 (1·0) 2·8 (0·3) 60·0 (5·5) 77·7 (6·9) NA
South E+ 65·3 (1·2)d 195·2 (13·8) 1·8 (0·2) 9·0 (1·0) 2·5 (0·1) 79·0 (4·6) 58·7 (1·7) 14·8 (0·8)

during the dry seasons of 1999 and 2000 coffee man-
agers began to remove epiphytes from shade trees. For
this study plantation managers removed the epiphytes
in accordance with our experimental design.
 
In 1999 and 2000 we established two experimental sites
located approximately 1 km apart at opposite sides of
the plantation (hereafter site: N, north; S, south). Each
site was divided into two 3-ha plots surrounded by
a matrix of shaded coffee with epiphytes. Plantation
workers removed all epiphytes from shade trees in one
of the two plots at each site (hereafter treatment: E+,
with epiphytes; E–, without epiphytes). Epiphyte removal
involved climbing on branches, which could be done
safely only during the dry season (February–May)
when epiphyte mats were not holding great amounts
of water. Workers tossed the removed epiphytes to the
ground and stacked them into small piles, where they
decomposed.
Vegetation surveys
Canopy management was not uniform throughout the
plantation, so variation among plots was expected. To
assess variation in vegetation variables among plots, we
randomly choose five 625-m2 (25 × 25-m) quadrats
per plot and measured shade cover with a spherical
densiometer (Lemmon 1957). We counted the number of
tree species and tree individuals (> 10 cm d.b.h.), and
calculated tree height per species. We measured coffee
shrub density as a percentage of ground cover in the
quadrat and we calculated mean coffee shrub height.
The dominant shade tree species in the plantation
was Inga jinicuil Schltdl. & Cham. Ex G. Don (Table 1),
which supported a typical vascular epiphyte commu-
nity (A. Cruz-Angón, unpublished data). We randomly
selected and measured 15 I. jinicuil trees ( > 10 cm
d.b.h.) in each plot and identified all vascular epiphytes
present in each tree. Observations were made with
© 2005 British
Ecological Society,
binoculars from the ground (Shaw & Bergstrom 1997).
Journal of Applied We established epiphyte richness on three plots; the
Ecology 42, southern plot without epiphytes (SE–) had no epiphytes
150–159 before the start of the study.
Shade cover was the only significantly different var-
iable between plots (F1,16 = 24·98, P = 0·001; Table 1) as
result of epiphyte removal. We recorded 40 species of
vascular epiphytes in the experimental plots out of a
total of 57 canopy dwelling species found on the farm.
Mean epiphyte richness per tree among plots did not
differ (F2,42 = 0·88, P = 0·42) but bird pollinated bro-
meliads were the most dominant epiphyte group.
Bird diversity and abundance
After a 3-month training period, bird surveys were
conducted in each plot by two observers. The results
presented in this paper cover observations taken from 1
August 2001 to 23 March 2002, which included the last
part of the breeding season (seven observation days
per plot) and most of the non-breeding season (16
observation days per plot). We alternated survey days
between sites and plots, covering one plot each day.
Each day one observer zig-zagged forwards through
the entire plot at a constant rate for 3·5 h (07:00 –10:30).
All birds seen or heard at a distance within 25 m of each
side of the observer were recorded. To minimize double-
counting we did not record birds that were behind
the observer or further than 25 m away. Species were
classified according to migratory status: (i) neotropical
migrants, species that breed in the neartic region and
winter in the neotropics; (ii) resident breeders, species
that breed in the coffee plantation; (iii) resident non-
breeders, Veracruz resident species only seen in coffee
plantations during the non-breeding season; and
(iv) residents, species seen all year in the area but not
observed breeding in coffee plantations. Common
and Latin names of bird species follow the American
Ornithologists’ Union (1998) and are presented in the
Appendix.
Epiphyte use by birds
Birds were classified according to their use of epiphytes
as (i) foraging substrate and (ii) nesting sites and mater-
ials. We used 2629 foraging observations gathered in
the same plantation from 1995 to 1998, and in addition
conducted 130 days of foraging observations (n = 2403)
on the experimental plots from May 2001 to March
153 Table 2. Bird species richness observed and expected for two pairs of experimental plots in a coffee plantation in Coatepec,
Epiphytes and birds Mexico. Mean expected species richness is based on rarefaction of 200 individuals for the breeding season and 900 individuals for
the non-breeding season. Total numbers of individuals observed are shown in parentheses after the observed species richness per
in coffee
season. Treatment, with epiphytes (E+), without epiphytes (E–)
plantations
Species richness per season
Breeding
Site Treatment Observed Estimated (SD)
North E+ 26 (280) 24·5 (1·0)
North E– 35 (249) 33·0 (1·2)
South E+ 40 (378) 33·9 (1·9)
South E– 33 (201) 32·9 (0·04)
2002. We recorded one foraging observation per indi-
vidual to maximize sample independence. We collected
data on bird species, height of the bird in the tree when
foraging, manoeuvre type, foraging substrate, tree
species and type of food obtained (nectar, arthropods,
fruit) (methods based on Remsen & Robinson 1990;
modified by Greenberg et al. 1999). When an individual
bird obtained a food item from an epiphyte, we identified
the family and species of epiphyte whenever possible.
We observed nesting behaviours in the coffee
plantation during the summers of 1995–99. Where we
were able to find and describe nests we calculated the
percentage of nests built in epiphyte substrates from
the total number of nests found per species.
 
We analysed seasons separately, because bird diversity
and abundance are much higher during the non-breeding
season when neotropical migrants are present.
Bird diversity and abundance
To assess the reliability of our surveys for recording
bird species richness, we carried out a rarefaction
analysis (Hurlbert 1971; James & Ratburn 1981) using
EcoSim v. 7 (Gottelli & Entsminger 2004). We set a
maximum number of individuals for the breeding
season to 200 and for the wintering season to 900,
taking into account the plot with the least number of
individuals observed (Table 2). To examine the effect
of epiphyte removal on bird abundance and species
richness, we conducted an  for a split-plot design
where observation day was considered a random block
that contained the site split into smaller experimental
plots (treatment). This allowed us to maximize the
power of test for the factor (treatment) in which we were
most interested (Sahai & Ageel 2000). Following tests
for normality and homoscedasticity we square-root
© 2005 British
Ecological Society, transformed the data (Zar 1999).
Journal of Applied To quantify the similarity of community composi-
Ecology 42, tion among plots, we generated a similarity matrix with
150–159 the Bray–Curtis coefficient. This index is calculated as:
Non-breeding
Total
Observed Estimated (SD) richness
54 (1227) 51·7 (1·3) 60
50 (1042) 48·6 (1·1) 62
54 (1238) 51·9 (1·3) 65
48 (977) 47·3 (0·8) 57
2Nj
CN =
Na + Nb
where Na is the total number of individuals in site A,
Nb is the total number of individuals in site B, and Nj is
the sum of the lower of the two abundances recorded
for species found in both sites. The index ranges from 1,
when communities are identical, to 0, when they are
entirely dissimilar (Magurran 1988). We then used a
multidimensional scaling algorithm (NMDS; Gauch,
Whittaker & Singer 1981; Gauch 1982; StatSoft Inc.
2000) to examine for clustering by community com-
position. We plotted the values obtained through this pro-
cedure in a scatter plot, where the proximity of the sites
is proportional to the degree of similarity. This allowed
us to detect meaningful underlying dimensions and
explain the observed similarities among the invest-
igated plots. The degree of correspondence between the
distances among points implied by the NMDS plot and
our similarity matrix is measured (inversely) by a stress
function. Finally, we carried out a Mantel’s test (Mantel
1967) to calculate the probability of acquiring a given
level of clustering by chance (Quinn & Keough 2002).
We conducted a Wilcoxon signed test to assess the
overall association of species within a treatment type.
The null hypothesis was that the signs (+ and −) and the
magnitude of the differences were equally distributed
(Zar 1999). We conducted a comparison of propor-
tions using chi-square tests to determine if the number
of individuals of a given species was significantly more
abundant in any of the treatments (with or without epi-
phytes). The null hypothesis was that individuals were
evenly distributed in both treatments. We performed
tests only for those species whose frequencies fulfilled
the test assumptions (Zar 1999). We assigned species to
one of three categories based on whether they were
significantly more abundant in either of the treatments:
(i) species more abundant on E– plots; (ii) species
evenly distributed among treatments (E– and E+); and
(iii) species significantly more abundant on E+. Signi-
ficance levels of the chi-square tests were corrected with
the Bonferroni method to counteract for the number of
simultaneous tests.
154
Epiphyte use by birds
A. Cruz-Angón &
R. Greenberg For those bird species where we had at least 20 foraging
observations (n = 33), we calculated the percentage
of foraging incidents that occurred on epiphytes.
We correlated this percentage with the percentage of
individuals of each of those species found in the E+
plots. With nesting observation data, we used a Kruskal–
Wallis test to determine if species that use epiphytes as
nest sites were significantly more abundant in E+ plots
than those not using epiphytes for nesting (Zar 1999).

Results

   

We recorded 91 bird species, of which 46 were neotro-
pical migrants and 45 were residents. Among the
residents, 29 were confirmed breeders in the study site
and 11 were year-round residents for which we had no
evidence of on-site breeding. The remaining five
resident species did not spend the breeding season in
the area (see the Appendix). Fig. 1. Rarefaction curves for the number of bird species
Total species richness was similar among plots and recorded in experimental plots in a coffee plantation in
ranged from 57 to 65. No one plot contained all 91 spe- Coatepec, Mexico. Mean species richness is shown at three
cies. During the breeding season, the NE+ plot had the points of individual resampling: (a) 50, 100 and 200 indi-
viduals for the breeding season; and (b) 300, 600 and 900
lowest richness (26 species) and the SE+ the highest (40
individuals for the non-breeding season. Data points are
species). During the non-breeding season, with-epiphyte mean expected richness, bars are 95% confidence intervals.
plots (NE+ and SE+) had more species than without- Experimental plots: north with epiphytes (diamonds), north
epiphyte plots (NE– and SE–). Estimated species rich- without epiphytes (squares), south with epiphytes (circles),
ness, as determined by rarefaction analysis, confirmed south without epiphytes (crosses).
this pattern for both seasons (Table 2). We present
rarefaction curves at three points of individual re-
sampling: 50, 100 and 200 individuals for the breeding
season, and 300, 600 and 900 individuals for the non-
breeding season (Fig. 1). Confidence intervals at 95%
overlapped widely among plots in both seasons, with
the exception of the NE+ plot, which remained the
lowest species diversity during the breeding season.
The  showed no significant differences in the
mean number of species observed within treatment in
any of the seasons (breeding season: F1,6 = 2·13, P = 0·19;
non-breeding season: F1,15 = 3·64, P = 0·07). The site
was not a significant factor during the breeding season
(F1,6 = 2·00, P = 0·20). During the non-breeding season,
however, mean species richness was significantly greater
(F1,15 = 6·67, P = 0·02) in northern plots (NE+ and NE−).
None the less, E– plots tended to have fewer species
than their E+ counterparts. There was no significant
site × treatment effects for either season (all P > 0·05).
The mean number of individuals observed was signi-
ficantly higher in E+ plots than in E– plots in both seasons
(breeding season: F1,6 = 43·61, P < 0·001; non-breeding
season: F1,15 = 8·52, P < 0·05). Neither site nor site ×
treatment effects were significant factors for either Fig. 2. Abundance of birds observed in four experimental
© 2005 British plots in a coffee plantation in Coatepec, Mexico, during the
Ecological Society,
season (P > 0·05; Fig. 2).
(a) breeding season and (b) non-breeding season. Sites: north
Journal of Applied Even though rarefaction analysis and  for species and south. Treatments: with epiphytes (E+); without epiphytes
Ecology 42, richness showed somewhat unexpected results between (E–). Data points represent mean number of individuals
150–159 treatments, the multidimensional scaling (NMDS) observed, and whiskers are 95% confidence intervals.
155
Epiphytes and birds
in coffee
plantations
Fig. 3. Ordination of two matched pairs of experimental plots, based on a multidimensional scaling analysis used to compare the
similarities of the studied plots during the breeding and non-breeding seasons (2001–02) in a coffee plantation in central Veracruz,
Mexico. Plots: north with epiphytes (NE+), north without epiphytes (NE–), south with epiphytes (SE+), south without epiphytes
(SE–). Stress = 0·006.
procedure showed a more consistent pattern. Two
dimensions were obtained (stress = 0·006): dimension 1
grouped plots according to the season (breeding vs. non-
breeding), and could be explained by the presence of
neotropical migrants that modify the structure of tropical
communities during the non-breeding season; dimension
2 grouped plots according to the treatment (with- or
without-epiphytes). This pattern was more evident for
the breeding season, whereas during the non-breeding
season community structure was very similar among
plots; however, equal treatments remained closer to each
other, which implied that plots with the same treatment
had similar bird community structures (Fig. 3). The
Mantel’s test showed a significant correlation (r = 0·39,
P < 0·01) between the similarity matrix and the matrix
produced by the NMDS procedure. These results indi-
cate that the grouping observed was not due to chance.
We found an overall tendency for bird species to occur
more commonly in E+ plots (Z = 2·76, P = 0·006).
Eighteen bird species were significantly more common
in E+ plots, while only three were more common in
E− plots. Seven migrant species were significantly more
abundant in E+ plots (χ2, d.f. = 1, P < 0·05). Among
residents, 11 species were significantly more abundant
in E+ plots (χ2, d.f. = 1, P < 0·05): two hummingbirds,
four breeding tanagers, three understorey breeding birds
and two non-breeding flycatchers. Only two migrants
(both granivores) and one breeding resident were more
abundant in E– plots (χ2, d.f. = 1, P < 0·05). When
Bonferroni correction was conducted, 11 of the 18
species that were more abundant in E+ plots remained
significant (P < 0·005), and only two of the three species
that where more abundant in E– plots remained sig-
nificant (see the Appendix).
   
© 2005 British
Ecological Society, Foraging
Journal of Applied
Ecology 42, We recorded 33 species (15 migrants and 18 residents)
150–159 using epiphytes as a foraging substrate (observed for-
aging incidents per species; n = 20). The percentage use
among species ranged from 3% to 74%. For example,
yellow-throated euphonias and the band-backed wrens
foraged on epiphytes in 74% of the observations. Wedge-
tailed sabrewings, grey catbirds and black-and-white
warblers were observed using epiphytes in about 50%
of foraging observations. Common bush-tanagers, the
most common resident in the plantation and the most
common species in the plots with epiphytes, foraged
in epiphytes around 30% of the time. Foraging guilds
using epiphytes included omnivores, insectivores and
nectarivores. We did not observe any granivorous
species foraging in epiphytes. The correlation between
the proportion of individuals found in with-epiphyte
plots and the percentage use of epiphytes as foraging
substrate was not significant (Fig. 4; r = 0·19, P = 0·07).
Nesting
Overall, species that used epiphytes as a nesting site or
for nesting materials were significantly more abundant
in E+ plots than those species that did not nest in
epiphytes (H1,26 = 3·42, P = 0·03). Among the 29 con-
firmed breeders, seven species used epiphytes as nesting
sites: band-backed wren, blue bunting, common bush-
tanager, squirrel cuckoo, tropical parula, white-winged
tanager and yellow-throated euphonia. The birds usually
built their nests inside epiphyte clumps, most commonly
bromeliads. The percentage use varied from 38% to 100%.
Three of the four breeding tanagers were particularly
dependent upon epiphyte clumps as nesting sites, using
them for 84–100% of their nests (see the Appendix).
The wedge-tailed hummingbirds and the azure-crowned
hummingbird used epiphytic lichens and mosses to ‘deco-
rate’ their nest. Band-backed wrens used Tillandsia spp.
with plumose seeds as a lining material for their nests.
Discussion
Our data suggest that the presence of epiphytes may
have direct and indirect effects not only on the canopy
156
A. Cruz-Angón &
R. Greenberg
Fig. 4. Correlation between the percentage use of epiphytes as a foraging substrate and the proportion of individuals observed
in the experimental plots with epiphytes (E+) in a coffee plantation in Central Veracruz, Mexico. Resident breeders (crosses),
residents with unknown breeding status (diamonds), residents non-breeders (circles), and neotropical migrants (triangles). r =
0·19, P = 0·07.
avifauna but on the understorey birds as well. The
four experimental plots differed only in the treatment
applied. This was confirmed by the vegetation surveys
where canopy cover, determined by epiphyte density,
was the only variable where plots differed significantly.
We did not find significant differences between treat-
ments in total species richness or mean number of bird
species observed, but there was an overall tendency for
bird species to occur in larger numbers in E+ plots.
The use of complementary biodiversity measurements,
such as similarity coefficients that take into account
both species richness and abundance, may reflect
ecological patterns in a more integral manner. Thus, we
were able to detect differences in bird abundance in a
number of forest-dependent taxa, which in turn had a
strong influence on overall community structure.
Focusing only on patterns of species presence and
absence may be too restricted when assessing diversity
in avian communities; changes in individual numbers
may be the first indication of local extinction (Ferraz
et al. 2003). The presence of a species does not imply
that a viable population is supported (Martin 1992;
Donovan et al. 1995; Robinson et al. 1995; Mas & Dietsch
2003). Even abundance measures do not address this
concern and further research is required to explore the
demographic consequences of management actions
such as epiphyte removal.
As we would expect, species more strongly associated
with epiphytes were less abundant in without-epiphyte
plots, which in turn may influence the structure of the
entire avian assemblage. For example, common bush-
tanagers were significantly more abundant in with-
epiphyte plots, as were all tanager species recorded in
our study site. Common bush-tanagers used epiphytes
as forage (30% of the time) and as a nesting substrate
(80% of the time). The use of epiphyte resources by this
© 2005 British
Ecological Society,
species has been described previously (Powell 1979;
Journal of Applied Isler & Isler 1987; Nadkarni & Matelson 1989; Sillett
Ecology 42, 1996; Richter 1998); however, this study confirms the
150–159 direct dependence and the importance of epiphyte
resources for these tanager species. Bush-tanagers play
an important role in mixed species flock structure and
function (Valburg 1992), hence their decline due to the
removal of epiphytes might affect the behaviour of
many other species.
Epiphytes may play a key role in reducing phenolog-
ical gaps in resources. In floristically impoverished
plantations such as commercial polycultures in the
central region of Veracruz, tree species of the genus
Inga comprise up to 70% of the shade trees. In this
type of plantation, epiphytes may become a critically
important food resource when tree hosts are not flower-
ing or fruiting (Williams-Linera 1997). Epiphytes such
as Anthurium scandens and Rhipsalis baccifera produce
large quantities of fruits that are regularly consumed
by resident tanagers and euphonias (i.e. common bush-
tanager, white-winged tanager and yellow-throated
euphonia; Snow 1981). Fruit production of these
epiphytes coincides with the birds’ breeding season
(April–September). Breeding requires high levels of
energy that can be obtained quickly and easily from the
epiphyte fruits (Greenberg 1981; Denslow, Moermond
& Levey 1986). In addition, the sequential flowering
of several bird-pollinated Tillandsia occurring in the
with-epiphyte plots at our study site guarantees a
year-round nectar supply for nectarivores such as
wedge-tailed hummingbirds (García-Franco, Martínez-
Burgoa & Pérez 2001).
Interestingly, we did not find a significant correlation
between the percentage use of epiphytes as a foraging
substrate and the proportion of individuals per species
in the with-epiphyte plots. This suggests that the use of
epiphytes as foraging substrate may not be the most
important factor explaining the presence of birds in
the with-epiphyte plots. None the less, the removal of
epiphytes modifies the canopy’s vertical structure by
decreasing foliage surface and biomass (Hoefestede,
Wolf & Benzig 1993). These changes may influence
encounter rates with prey, prey accessibility and ener-
getic costs of attacking and capturing prey (Gradwhol
157 & Greenberg 1980; Robinson & Holmes 1982; Schmidt
Epiphytes and birds 1998; Whelan 2001). Furthermore, the removal of
in coffee epiphytes might disrupt the life cycle of arthropods
plantations predated by birds, thus further limiting food availability
(Kitching et al. 1997).
The significant relationship between the species
that use epiphytes as a nesting site and their greater
abundance in plots with epiphytes confirms the close
dependence of resident species upon epiphyte resources.
The use of epiphytes as a nesting site may give addi-
tional concealment against potential predators. On the
other hand, some species that were more abundant in
the E+ plots did not utilize epiphytes directly. This was
particularly true for migrant species such as olive-sided
flycatchers, solitary vireos, summer tanagers and
Tennessee warblers, which did not forage on epiphytes
but were more abundant in the E+ plots. Some species
may have preferred E+ plots because they use epiphytes
as a simple cue to assess appropriate (forest) habitat
(Lack 1933).
In addition, some understorey resident breeders
(golden-crowned warbler, spot-breasted wren and rusty
sparrow), which neither forage nor nest in epiphytes,
were more abundant in the E+ plots. Epiphytes may
play an indirect role in maintaining the abundance of
many species. Such indirect effects would be undetect-
able from observational studies on the use of epiphytes
by birds, for example epiphyte influence on micro-
climate. Lorr (2001), working on our experimental
plots, found that, as a consequence of epiphyte removal,
canopy cover and soil moisture were reduced while stem-
flow and rain through-fall increased. Thus, more water
reached the ground in less time but evaporated faster.
During the breeding season, increases in running water
could flood nests and affect ground nesters such as
golden-crowned warblers and rusty sparrows. More-
over, unexpected changes in the microclimate could
influence the abundance and diversity of arthropods,
not only in the canopy but in the understorey arthro-
pod fauna as well, and important prey species may
become less abundant and less accessible (Stuntz 2001;
A. Cruz-Angón & Greenberg, unpublished data). In
addition, greater canopy openness due to epiphyte
removal may increase birds’ detection by potential
predators. Several authors have demonstrated that
individual fitness can be affected by environmental
factors such as extreme temperature, food shortage
and predation (Calder 1984; Peters 1986; Nager & Zandt
1994; Carrascal et al. 1998).
As a consequence of increased canopy openness and
greater light incidence in the without-epiphyte plots,
weeds might proliferate. This could explain the signi-
ficantly higher abundance of weed-dependent granivores
such as indigo buntings and painted buntings in
without-epiphyte plots. However, weeds are an ephem-
© 2005 British
Ecological Society,
eral resource in coffee plantations because they are
Journal of Applied regularly removed from the understorey. The only
Ecology 42, resident species that was significantly more abundant
150–159 in the without-epiphyte plot was the golden-fronted
woodpecker, which paradoxically used epiphytes as a
foraging substrate about 50% of the time. The higher
abundance of this species could be due to epiphyte removal
increasing woodpecker accessibility to tree bark. This
might be advantageous for a primary cavity nesting species
as epiphyte-free trees would improve tree selection.

This study has provided experimental evidence of the
importance of epiphytes in supporting bird abundance
and diversity in coffee plantations, particularly forest-
dependent species. Although focused on coffee planta-
tions, these findings might also indicate the ecological
importance of epiphytes for birds in other ecosystems,
such as tropical montane cloud forests. Our results sup-
port the use of the positive epiphyte management and
validate the use of this criterion to certify shade-grown
coffee. Epiphytes are an important resource for birds,
not only because they provide critical resources such
as food and nest materials, but also because epiphytes
mediate in microclimate regulation, and may offer
refuge and cover to the birds. The long-term effects of
epiphyte removal still need to be assessed. Although
coffee plantations where epiphyte removal is practised
provide a unique opportunity to research direct and
indirect effects of this practice, the management should
not be promoted. Given the negative impacts of this
technique on birds it should be actively discouraged.
The shade-grown coffee certification scheme provides a
practical means of achieving this.
Acknowledgements
We thank A. Martínez-Fernández, P. Bichier-Garrido
and B. Lorr for assistance with fieldwork. The Martínez
family and plantation manager R. Monge gave generous
access to their coffee plantation. V.J. Sosa-Fernández,
T.S. Sillett and A. Flores-Palacios provided statistical
advice, and comments on the manuscript. J.G. García-
Franco, V. Rico-Gray, M. Coro-Arizmendi, E.I. Paul,
S.M. Philpot, A. Vovides, J.A. González-Astorga, P.
Bichier-Garrido, C.J. Whelan and K. Hammer improved
the manuscript with their comments and corrections.
Funding to A. Cruz-Angón was provided by CONACYT
(scholarship 128767), Smithsonian Institution Visiting
Award 2002–03 and Departamento de Ecología Fun-
cional of the Instituto de Ecología and grants from the
National Geographic Society and Scholarly Studies
Fund of the Smithsonian Institution to R. Greenberg.
This study constitutes partial fulfilment of A. Cruz-
Angón’s PhD in Ecology and Natural Resources
Management at the Instituto de Ecología, AC.
Supplementary material
The following material is available from http://
www.blackwellpublishing.com/products/journals/
suppmat/JPE/JPE983/JPE983sm.htm.
158 Appendix. Abundance and epiphyte use by bird species
A. Cruz-Angón & recorded in experimental plots in a coffee plantation in
R. Greenberg Coatepec, Mexico.
References
Aguilar-Ortiz, F. (1982) Estudio ecológico de las aves del
cafetal. Estudios de Ecología en el agroecosistema cafetalero
(ed. E. Avila Jiménez), pp. 103–128. INIREB, Xalapa, Ver-
acruz, Mexico.
American Ornithologists’ Union (1998) Check-List of North
American Birds, 7th edn. American Ornithologists’ Union,
Washington, DC.
Calder, W.A. III (1984) Size, Function and Life History. Harvard
University Press, Cambridge, MA.
Carrascal, L.M., Senar, J.C., Mozetich, I., Uribe, F. & Domenech, J.
(1998) Interactions among environmental stress, body
condition, nutritional status, and dominance in great tits.
Auk, 115, 727–738.
Dean, W.R.J., Milton, S.J. & Siegfried, W.R. (1990) Dispersal
of seeds as nest material by birds in semiarid Karoo shrub-
land. Ecology, 71, 1299 –1306.
Denslow, J.S., Moermond, T.C. & Levey, D.J. (1986) Spatial
components of fruit display in understorey trees and shrubs.
Frugivores and Seed Dispersal (eds A. Estrada & T.H.
Flemning), pp. 37– 44. Dr W. Junk Publishers, Dordrecht,
the Netherlands.
Donovan, T.M., Thompson, F.R. III, Faaborg, J. & Probst, J.R.
(1995) Reproductive success of migratory birds in habitat
sources and sinks. Conservation Biology, 9, 1380 –1395.
Ferraz, G., Russell, G.J., Stouffer, P.C., Bierregaard, R.O. Jr,
Pimm, S.L. & Lovejoy, T.E. (2003) Rates of species loss
from Amazonian forest fragments. Proceedings of the National
Academy of Science USA, 100, 14070 –14073.
García-Franco, J.G., Martínez-Burgoa, D. & Pérez, T.M. (2001)
Hummingbird flower mites and Tillandsia spp. (Bromeli-
acaeae): polyphagy in a cloud forest of Veracruz, Mexico.
Biotropica, 33, 538 –542.
Gauch, H.J. Jr (1982) Multivariate Analysis in Community
Ecology. Cambridge University Press, Cambridge, UK.
Gauch, H.J. Jr, Whittaker, R.H. & Singer, S.B. (1981) A
comparative study of nonmetric ordinations. Journal of
Ecology, 69, 135 –152.
Gentry, A.W. & Dodson, C.H. (1987) Diversity and biogeo-
graphy of neotropical vascular epiphytes. Annals of Missouri
Botanical Garden, 74, 205 –233.
Gottelli, N.J. & Entsminger, G.L. (2004) Ecosim: Null Models
Software for Ecology, Version 7·0. Acquired Intelligence Inc.
& Kesey-Bear. Burlington, YT, USA.
http:// homepages.together.net /∼gentsim / ecosim.htm.
Gradwhol, J. & Greenberg, R. (1980) The formation of antwren
flocks on Barro Colorado island, Panama. Auk, 97, 385–
395.
Greenberg, R. (1981) Frugivory in some migrant tropical
forest wood warblers. Biotrópica, 13, 215 –223.
Greenberg, R., Bichier, P., Cruz-Angón, A. & Reitsma, R.
(1997) Bird populations in shade coffee plantations in
Central Guatemala. Conservation Biology, 11, 448 – 459.
Greenberg, R., Bichier, P. & Sterling, J. (1997) Bird popula-
tions in rustic and planted shade coffee plantations of eastern
Chiapas. Biotropica, 29, 501–514.
Greenberg, R., Pravosudov, V., Sterling, J., Kozlenko, A. &
Kontorshikov, V. (1999) Divergence in foraging behavior of
foliage-gleaning birds. Oecologia, 120, 451– 462.
Hoefestede, R.G.M., Wolf, J.H.D. & Benzig, D.H. (1993)
© 2005 British
Epiphytic biomass and nutrient status of a Colombian
Ecological Society,
upper montane rain forest. Selbyana, 14, 37– 45.
Journal of Applied
Hurlbert, S.H. (1971) The nonconcept of species diversity:
Ecology 42, a critique and alternative parameters. Ecology, 52, 577–
150–159 586.
Isler, L.M. & Isler, P.R. (1987) The Tanagers: Natural History,
Distribution, and Identification. Smithsonian Institution Press,
Washington, DC.
James, C.D. & Ratburn, S. (1981) Rarefaction, relative abund-
ance and diversity of avian communities. Auk, 98, 785–800.
Johnson, M.D. (2000) Effects of shade-tree species and crop
structure on the winter arthropod and bird communities in
a Jamaican shade coffee plantation. Biotropica, 32, 133–145.
Jones, J., Ramoni-Perazzi, P., Carruthers, E.H. & Robertson, R.J.
(2000) Sociality and foraging behavior of the Cerulean
warbler in Venezuelan shade-coffee plantations. Condor,
102, 958 –962.
Kitching, R.L., Mitchell, H., Morse, G. & Thebaud, C. (1997)
Determinants of species richness in assemblages of canopy
arthropods in rainforests. Canopy Arthropods (eds N.E. Stork,
J. Adis & R.K. Didham), pp. 131–150. Chapman & Hall,
London, UK.
Lack, D. (1933) Habitat selection in birds. Journal of Animal
Ecology, 2, 239 –262.
Lemmon, P.E. (1957) A new instrument for measuring forest
overstorey density. Journal of Forestry, 55, 667–668.
Lorr, B. (2001) Examining the effects of epiphyte removal on
the hydrology of a shade coffee ecosystem. Senior Thesis.
University of Columbia, New York, NY.
Magurran, A.E. (1988) Ecological Diversity and its Measurement.
Princeton University Press, Princeton, NJ.
Mantel, N. (1967) The detection of disease clustering and
generalized detection approach. Cancer Research, 27, 1627–
1637.
Martin, T.E. (1992) Breeding productivity considerations:
what are the appropriate habitat features for management?
Ecology and Conservation of Neotropical Migrant Land-
birds (eds J.M. Hagan III & D.W. Johnston), pp. 455–473.
Smithsonian Institute Press, Washington, DC.
Mas, A.H. (1999) Butterflies as biodiversity indicators and
shade coffee certification in Chiapas, Mexico. MS Thesis.
University of Michigan, Ann Arbor, MI.
Mas, A.H. & Dietsch, T. (2003) An index of management
intensity for coffee agroecosystems to evaluate butterfly
species richness. Ecological Applications, 13, 1491–1501.
Moguel, P. & Toledo, V.M. (1999) Biodiversity conservation
in traditional coffee systems in Mexico. Conservation Biology,
13, 1–12.
Nadkarni, N.M. & Matelson, T.J. (1989) Bird use of epiphyte
resources in neotropical trees. Condor, 91, 891–907.
Nadkarni, N.M., Merwin, M.C. & Nieder, J. (2001) Forest
canopies, plant diversity. Encyclopedia of Diversity (ed.
S. A. Levin), pp. 27–40. Academic Press, London.
Nager, R.G. & Zandt, H.S. (1994) Variation in egg size in
great tits. Ardea, 82, 315 –328.
Perfecto, I. & Armbrecht, I. (2002) The coffee agroecosystem
in the neotropics: combining ecological and economic goals.
Tropical Agroecosystems (ed. J. Vandermeer), pp. 159–194.
CRC Press, Boca-Raton, FLA.
Perfecto, I., Rice, R.A., Greenberg, R. & Van Der Voort, M.E.
(1996) Shade coffee: a disappearing refuge for biodiversity.
Bioscience, 46, 598 – 607.
Peters, R.H. (1986) The Ecological Implications of Body Size.
Cambridge University Press, Cambridge, MA.
Powell, G.V.N. (1979) Structure and dynamics of interspecific
flocks in a neotropical mid-elevation forest. Auk, 96, 375–
390.
Quinn, G.P. & Keough, M.J. (2002) Experimental Design and
Data Analysis for Biologists. Cambridge University Press,
Cambridge, UK.
Remsen, J.V. Jr (1985) Community organization and ecology
of birds of high elevation humid forest of the Bolivian Andes.
Ornithological Monographs, 36, 733 –756.
Remsen, J.V. Jr & Robinson, S.K. (1990) A classification
scheme for foraging behavior of birds in terrestrial habitats.
Studies in Avian Biology, 13, 144 –160.
159 Richter, C. (1998) Breeding success and nest sites of the common
Epiphytes and birds bush-tanager (Chlorospingus ophthalmicus ophthalmicus)
in shaded coffee plantations of Veracruz, México. MS Thesis.
in coffee
University of Michigan, Ann Arbor, MI.
plantations Robinson, S.K. & Holmes, R.T. (1982) Foraging behavior of
forest birds: the relationships among search tactics, diet,
and habitat structure. Ecology, 63, 1918 –1931.
Robinson, S.K., Thompson, F.R. III, Donovan, T.M.,
Whitehead, D. & Faaborg, J. (1995) Regional forest
fragmentation and the nesting success of migratory birds.
Science, 267, 1987–1990.
Sahai, H. & Ageel, M.I. (2000) The Analysis of Variance: Fixed
Random and Mixed Models. Birkhäuser, Boston, MA.
Schmidt, K.A. (1998) Consequences of partially directed
search efforts. Evolutionary Ecology, 12, 263 –277.
Shaw, J.D. & Bergstrom, D.M. (1997) A rapid assessment
technique of vascular epiphyte diversity at forest and
regional levels. Selbyana, 18, 195 –199.
Sillett, T.S. (1996) Foraging ecology of epiphyte-searching
insectivorous birds in Costa Rica. Condor, 96, 866 – 877.
Sillett, T.S., James, A. & Sillett, K. (1997) Bromeliad foraging
specialization and diet selection of Pseudocolaptes lawrencii
(Furnariidae). Ornithological Monographs, 48, 733–742.
Snow, D.W. (1981) Tropical frugivorous birds and their food
resources: a world survey. Biotropica, 13, 1–14.
Solis, M.L. (2002) Estudio poblacional y biología reproductiva
de las orquídeas silvestres de un cafetal de la Orduña, Veracruz,
México. Senior Thesis. Universidad de la Americas, Puebla,
Mexico.
StatSoft Inc. (2000) STATISTICA for Windows. StatSoft
Inc., Tulsa, OK.
Stuntz, S. (2001) The influence of epiphytes on arthropods in the
tropical forest canopy. PhD Thesis. University of Wüuzburg,
Wüuzburg, Germany.
© 2005 British
Ecological Society,
Journal of Applied
Ecology 42,
150–159
View publication stats
Valburg, L.K. (1992) Flocking and frugivory: the effect of
social groupings on resource use in the common bush-
tanager. Condor, 94, 358 –363.
Warkentin, I.G., Greenberg, R. & Salgado-Ortiz, J. (1995)
Songbird use of gallery woodlands in recently cleared and
older settled landscapes of the Selva Lacandona, Chiapas,
Mexico. Conservation Biology, 9, 1095 –1106.
Whelan, C.J. (2001) Foliage structure influences foraging of
insectivorous forest birds: an experimental study. Ecology,
82, 219 –231.
Williams-Linera, G. (1997) Phenology of deciduous and
broadleaved-evergreen tree species in a Mexican tropical
lower montane forest. Global Ecology and Biogeography
Letters, 6, 115 –127.
Williams-Linera, G. (2002) Tree species richness comple-
mentary, disturbance and fragmentation in a Mexican tropical
montane cloud forest. Biodiversity and Conservation, 11,
1825 –1843.
Williams-Linera, G., Manson, R.H. & Isunza, E.V. (2002) La
fragmentación del bosque mesófilo de montaña y patrones
de uso del suelo en la región oeste de Xalapa, Veracruz,
México. Madera y Bosques, 8, 73 – 89.
Wunderle, J.M. & Latta, S.C. (1996) Avian abundance in sun
and shade coffee plantations and remnant pine forest in
the Cordillera Central, Dominican Republic. Ornitología
Neotropical, 7, 19 –34.
Wunderle, J.M. & Waide, R.B. (1993) Distribution of over-
wintering neartic migrants in the Bahamas and Greater
Antilles. Condor, 95, 904 –933.
Zar, J.H. (1999) Biostatistical Analysis. Prentice Hall Inc.,
Upper Saddle River, NJ.
Received 19 January 2004; final copy received 10 September
2004